{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T05:59:22Z","timestamp":1772258362566,"version":"3.50.1"},"reference-count":82,"publisher":"Copernicus GmbH","issue":"5","license":[{"start":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T00:00:00Z","timestamp":1583452800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biogeosciences"],"abstract":"<jats:p>Abstract. Sponges are commonly known as general nutrient providers for the marine\necosystem, recycling organic matter into various forms of bioavailable\nnutrients such as ammonium and nitrate. In this study we challenge this\nview. We show that nutrient removal through microbial denitrification is a\ncommon feature in six cold-water sponge species from boreal and Arctic\nsponge grounds. Denitrification rates were quantified by incubating sponge\ntissue sections with 15NO3--amended oxygen-saturated\nseawater, mimicking conditions in pumping sponges, and de-oxygenated\nseawater, mimicking non-pumping sponges. It was not possible to detect any rates of anaerobic ammonium\noxidation (anammox) using incubations with 15NH4+. Denitrification rates of the different sponge species ranged\nfrom below detection to 97\u2009nmol\u2009N\u2009cm\u22123 sponge\u2009d\u22121 under oxic\nconditions, and from 24 to 279\u2009nmol\u2009N\u2009cm\u22123 sponge\u2009d\u22121 under\nanoxic conditions. A positive relationship between the highest potential rates of\ndenitrification (in the absence of oxygen) and the species-specific\nabundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for\ndenitrification, suggests that the denitrifying community in these sponge\nspecies is active and prepared for denitrification. The lack of a lag phase\nin the linear accumulation of the 15N-labelled N2 gas in any of\nour tissue incubations is another indicator for an active community of\ndenitrifiers in the investigated sponge species. Low rates for coupled nitrification\u2013denitrification indicate that also under\noxic conditions, the nitrate used to fuel denitrification rates was derived rather\nfrom the ambient seawater than from sponge nitrification. The lack of nifH\ngenes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that\nthe nitrogen cycle is not closed in the sponge grounds. The denitrified\nnitrogen, no matter its origin, is then no longer available as a nutrient\nfor the marine ecosystem. These results suggest a high potential denitrification capacity of deep-sea\nsponge grounds based on typical sponge biomass on boreal and Arctic sponge\ngrounds, with areal denitrification rates of 0.6\u2009mmol\u2009N\u2009m\u22122\u2009d\u22121 assuming non-pumping sponges and still 0.3\u2009mmol\u2009N\u2009m\u22122\u2009d\u22121\nassuming pumping sponges. This is well within the range of denitrification\nrates of continental shelf sediments. Anthropogenic impact and global change\nprocesses affecting the sponge redox state may thus lead to deep-sea\nsponge grounds changing their role in marine ecosystem from being mainly\nnutrient sources to becoming mainly nutrient sinks.<\/jats:p>","DOI":"10.5194\/bg-17-1231-2020","type":"journal-article","created":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T01:26:14Z","timestamp":1583457974000},"page":"1231-1245","source":"Crossref","is-referenced-by-count":27,"title":["Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges"],"prefix":"10.5194","volume":"17","author":[{"given":"Christine","family":"Rooks","sequence":"first","affiliation":[]},{"given":"James Kar-Hei","family":"Fang","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6518-4520","authenticated-orcid":false,"given":"P\u00e5l Tore","family":"M\u00f8rkved","sequence":"additional","affiliation":[]},{"given":"Rui","family":"Zhao","sequence":"additional","affiliation":[]},{"given":"Hans Tore","family":"Rapp","sequence":"additional","affiliation":[]},{"given":"Joana R.","family":"Xavier","sequence":"additional","affiliation":[]},{"given":"Friederike","family":"Hoffmann","sequence":"additional","affiliation":[]}],"member":"3145","published-online":{"date-parts":[[2020,3,6]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"Archer, S. K., Stevens, J. L., Rossi, R. E., Matterson, K. O., and Layman,\nC. A.: Abiotic conditions drive significant variability in nutrient\nprocessing by a common Caribbean sponge, Ircinia felix, Limnol. Oceanogr., 62,\n1783\u20131793, https:\/\/doi.org\/10.1002\/lno.10533, 2017.","DOI":"10.1002\/lno.10533"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Baumann, B., Snozzi, M., Zehnder, A. J., and Van Der Meer, J. R.: Dynamics\nof denitrification activity of Paracoccus denitrificans in continuous\nculture during aerobic-anaerobic changes, J. Bacteriol., 178,\n4367\u20134374, https:\/\/doi.org\/10.1128\/jb.178.15.4367-4374.1996, 1996.","DOI":"10.1128\/jb.178.15.4367-4374.1996"},{"key":"ref3","doi-asserted-by":"crossref","unstructured":"Baumann, B., Snozzi, M., Van Der Meer, J. R., and Zehnder, A. J. B.:\nDevelopment of stable denitrifying cultures during repeated\naerobic-anaerobic transient periods, Water Res., 31, 1947\u20131954, https:\/\/doi.org\/10.1016\/S0043-1354(97)00053-5, 1997.","DOI":"10.1016\/S0043-1354(97)00053-5"},{"key":"ref4","doi-asserted-by":"crossref","unstructured":"Baumberger, T., Fr\u00fch-Green, G. L., Thorseth, I. H., Lilley, M. D.,\nHamelin, C., Bernasconi, S. M., Okland, I. E., and Pedersen, R. B.: Fluid\ncomposition of the sediment-influenced Loki's Castle vent field at the\nultra-slow spreading Arctic Mid-Ocean Ridge, Geochim. Cosmochim.\nAc., 187, 156\u2013178, https:\/\/doi.org\/10.1016\/j.gca.2016.05.017, 2016.","DOI":"10.1016\/j.gca.2016.05.017"},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"Bayer, K., Schmitt, S., and Hentschel, U.: Physiology, phylogeny and in situ\nevidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba, Environ. Microbiol., 10, 2942\u20132955,\nhttps:\/\/doi.org\/10.1111\/j.1462-2920.2008.01582.x, 2008.","DOI":"10.1111\/j.1462-2920.2008.01582.x"},{"key":"ref6","doi-asserted-by":"crossref","unstructured":"Bayer, K., Moitinho-Silva, L., Brummer, F., Cannistraci, C. V., Ravasi, T.,\nand Hentschel, U.: GeoChip-based insights into the microbial functional gene\nrepertoire of marine sponges (high microbial abundance, low microbial\nabundance) and seawater, Fems Microbiol. Ecol., 90, 832\u2013843,\nhttps:\/\/doi.org\/10.1111\/1574-6941.12441, 2014.","DOI":"10.1111\/1574-6941.12441"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Bell, J. J., McGrath, E., Biggerstaff, A., Bates, T., Bennett, H., Marlow,\nJ., and Shaffer, M.: Sediment impacts on marine sponges, Mar. Pollut. Bull.,\n94, 5\u201313, https:\/\/doi.org\/10.1016\/j.marpolbul.2015.03.030, 2015.","DOI":"10.1016\/j.marpolbul.2015.03.030"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Bulow, S. E., Rich, J. J., Naik, H. S., Pratihary, A. K., and Ward, B. B.:\nDenitrification exceeds anammox as a nitrogen loss pathway in the Arabian\nSea oxygen minimum zone, Deep-Sea Res. Pt. I, 57, 384\u2013393, https:\/\/doi.org\/10.1016\/j.dsr.2009.10.014, 2010.","DOI":"10.1016\/j.dsr.2009.10.014"},{"key":"ref9","doi-asserted-by":"crossref","unstructured":"Card\u00e9nas, P., Rapp, H. T., Klitgaard, A. B., Best, M., Thollesson, M., and\nTendal, O. S.: Taxonomy, biogeography and DNA barcodes of Geodia species\n(Porifera, Demospongiae, Tetractinellida) in the Atlantic boreo-arctic\nregion, Zool. J. Linn. Soc.-Lond., 169, 251\u2013311, https:\/\/doi.org\/10.1111\/zoj.12056, 2013.","DOI":"10.1111\/zoj.12056"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Chen, J. W. and Strous, M.: Denitrification and aerobic respiration, hybrid\nelectron transport chains and co-evolution, Biochim. Biophys.\nAc., 1827, 136\u2013144, https:\/\/doi.org\/10.1016\/j.bbabio.2012.10.002, 2013.","DOI":"10.1016\/j.bbabio.2012.10.002"},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"Cleary, D. F. R., de Voogd, N. J., Polonia, A. R. M., Freitas, R., and\nGomes, N. C. M.: Composition and Predictive Functional Analysis of Bacterial\nCommunities in Seawater, Sediment and Sponges in the Spermonde Archipelago,\nIndonesia, Microb. Ecol., 70, 889\u2013903, https:\/\/doi.org\/10.1007\/s00248-015-0632-5, 2015.","DOI":"10.1007\/s00248-015-0632-5"},{"key":"ref12","doi-asserted-by":"crossref","unstructured":"Corredor, J., Wilkinson, C., P. Vicente, V., Morell, J., and Otero Morales,\nE.: Nitrate release by Caribbean reef sponges, 114\u2013120, 1988.","DOI":"10.4319\/lo.1988.33.1.0114"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"de Goeij, J. M., van Oevelen, D., Vermeij, M. J. A., Osinga, R., Middelburg,\nJ. J., and de Goeij, A. F. P. M.: Surviving in a marine desert: the sponge\nloop retains resources within coral reefs, Science, 342, 108\u2013110, https:\/\/doi.org\/10.1126\/science.1241981, 2013.","DOI":"10.1126\/science.1241981"},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Diaz, M. C. and Ward, B. B.: Sponge-mediated nitrification in tropical\nbenthic communities, Mar. Ecol. Prog. Ser., 156, 97\u2013107, https:\/\/doi.org\/10.3354\/meps156097, 1997.","DOI":"10.3354\/meps156097"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"Fang, J. K. H., Rooks, C. A., Krogness, C. M., Kutti, T., Hoffmann, F., and\nBannister, R. J.: Impact of particulate sediment, bentonite and barite\n(oil-drilling waste) on net fluxes of oxygen and nitrogen in Arctic-boreal\nsponges, Environ. Pollut., 238, 948\u2013958, https:\/\/doi.org\/10.1016\/j.envpol.2017.11.092,\n2018.","DOI":"10.1016\/j.envpol.2017.11.092"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Feng, G. and Li, Z.: Carbon and Nitrogen Metabolism of Sponge Microbiome,\nin: Symbiotic Microbiomes of Coral Reefs Sponges and Corals, edited by: Li,\nZ., Springer, Dordrecht, 145\u2013169, 2019.","DOI":"10.1007\/978-94-024-1612-1_9"},{"key":"ref17","doi-asserted-by":"crossref","unstructured":"Fiore, C. L., Jarett, J. K., Olson, N. D., and Lesser, M. P.: Nitrogen\nfixation and nitrogen transformations in marine symbioses, Trend.\nMicrobiol., 18, 455\u2013463, https:\/\/doi.org\/10.1016\/j.tim.2010.07.001, 2010.","DOI":"10.1016\/j.tim.2010.07.001"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Fiore, C. L., Baker, D. M., and Lesser, M. P.: Nitrogen Biogeochemistry in\nthe Caribbean Sponge, Xestospongia muta: A Source or Sink of Dissolved Inorganic Nitrogen?,\nPLOS ONE, 8, e72961, https:\/\/doi.org\/10.1371\/journal.pone.0072961, 2013.","DOI":"10.1371\/journal.pone.0072961"},{"key":"ref19","doi-asserted-by":"crossref","unstructured":"Fiore, C. L., Labrie, M., Jarettt, J. K., and Lesser, M. P.: Transcriptional\nactivity of the giant barrel sponge, Xestospongia muta Holobiont: molecular\nevidence for metabolic interchange, Front. Microbiol., 6, 1\u201318,\nhttps:\/\/doi.org\/10.3389\/fmicb.2015.00364, 2015.","DOI":"10.3389\/fmicb.2015.00364"},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Folkers, M. and Rombouts, T.: Sponges Revealed: A Synthesis of Their\nOverlooked Ecological Functions Within Aquatic Ecosystems, in: YOUMARES 9 \u2013\nThe Oceans: Our Research, Our Future, edited by: Jungblut, S., Liebich, V., and Bode-Dalby, M.,\nSpringer, Cham, 181\u2013193, 2020.","DOI":"10.1007\/978-3-030-20389-4_9"},{"key":"ref21","doi-asserted-by":"crossref","unstructured":"Han, M. Q., Liu, F., Zhang, F. L., Li, Z. Y., and Lin, H. W.: Bacterial and\nArchaeal Symbionts in the South China Sea Sponge Phakellia fusca: Community\nStructure, Relative Abundance, and Ammonia-Oxidizing Populations, Mar.\nBiotechnol., 14, 701\u2013713, doi10.1007\/s10126-012-9436-5, 2012.","DOI":"10.1007\/s10126-012-9436-5"},{"key":"ref22","doi-asserted-by":"crossref","unstructured":"Han, M. Q., Li, Z. Y., and Zhang, F. L.: The Ammonia Oxidizing and\nDenitrifying Prokaryotes Associated with Sponges from Different Sea Areas,\nMicrob. Ecol., 66, 427\u2013436, https:\/\/doi.org\/10.1007\/s00248-013-0197-0, 2013.","DOI":"10.1007\/s00248-013-0197-0"},{"key":"ref23","doi-asserted-by":"crossref","unstructured":"Hoer, D. R., Tommerdahl, J. P., Lindquist, N. L., and Martens, C. S.:\nDissolved inorganic nitrogen fluxes from common Florida Bay (USA) sponges,\nLimnol. Oceanogr., 63, 2563\u20132578, https:\/\/doi.org\/10.1002\/lno.10960, 2018.","DOI":"10.1002\/lno.10960"},{"key":"ref24","doi-asserted-by":"crossref","unstructured":"Hoffmann, F., Rapp, H., Z\u00f6ller, T., and Reitner, J.: Growth and\nregeneration in cultivated fragments of the boreal deep water sponge Geodia barretti Bowerbank, 1858 (Geodiidae, Tetractinellida, Demospongiae), 109\u2013118, 2003.","DOI":"10.1016\/S0168-1656(02)00258-4"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"Hoffmann, F., Larsen, O., Thiel, V., Rapp, H. T., Pape, T., Michaelis, W.,\nand Reitner, J.: An Anaerobic World in Sponges, Geomicrobiol. J., 22,\n1\u201310, https:\/\/doi.org\/10.1080\/01490450590922505, 2005.","DOI":"10.1080\/01490450590922505"},{"key":"ref26","doi-asserted-by":"crossref","unstructured":"Hoffmann, F., R\u00f8y, H., Bayer, K., Hentschel, U., Pfannkuchen, M.,\nBr\u00fcmmer, F., and de Beer, D.: Oxygen dynamics and transport in the\nMediterranean sponge Aplysina aerophoba, Mar. Biol., 153, 1257\u20131264, https:\/\/doi.org\/10.1007\/s00227-008-0905-3, 2008.","DOI":"10.1007\/s00227-008-0905-3"},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"Hoffmann, F., Radax, R., Woebken, D., Holtappels, M., Lavik, G., Rapp, H.\nT., Schl\u00e4ppy, M.-L., Schleper, C., and Kuypers, M. M. M.: Complex\nnitrogen cycling in the sponge Geodia barretti, Environ. Microbiol.,\n11, 2228\u20132243, https:\/\/doi.org\/10.1111\/j.1462-2920.2009.01944.x, 2009.","DOI":"10.1111\/j.1462-2920.2009.01944.x"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"Holtappels, M., Lavik, G., Jensen, M. M., and Kuypers, M. M. M.: Chapter ten\n\u2013 15N-Labeling Experiments to Dissect the Contributions of Heterotrophic\nDenitrification and Anammox to Nitrogen Removal in the OMZ Waters of the\nOcean, in: Methods in Enzymology, edited by: Klotz, M. G., Academic Press,\n223\u2013251, 2011.","DOI":"10.1016\/B978-0-12-381294-0.00010-9"},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"Hughes, D. J. and Gage, J. D.: Benthic metazoan biomass, community\nstructure and bioturbation at three contrasting deep-water sites on the\nnorthwest European continental margin, Prog. Oceanogr., 63, 29\u201355,\nhttps:\/\/doi.org\/10.1016\/j.pocean.2004.09.002, 2004.","DOI":"10.1016\/j.pocean.2004.09.002"},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"Jim\u00e9nez, E. and Ribes, M.: Sponges as a source of dissolved inorganic\nnitrogen: Nitrification mediated by temperate sponges, Limnol. Oceanogr., 52,\n948\u2013958, https:\/\/doi.org\/10.4319\/lo.2007.52.3.0948, 2007.","DOI":"10.4319\/lo.2007.52.3.0948"},{"key":"ref31","doi-asserted-by":"crossref","unstructured":"Kahn, A. S., Yahel, G., Chu, J. W. F., Tunnicliffe, V., and Leys, S. P.:\nBenthic grazing and carbon sequestration by deep-water glass sponge reefs,\nLimnol. Oceanogr., 60, 78\u201388, https:\/\/doi.org\/10.1002\/lno.10002, 2015.","DOI":"10.1002\/lno.10002"},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"Keesing, J. K., Strzelecki, J., Fromont, J., and Thomson, D.: Sponges as\nimportant sources of nitrate on an oligotrophic continental shelf, Limnol. Oceanogr., 58,\n1947\u20131958, https:\/\/doi.org\/10.4319\/lo.2013.58.6.1947, 2013.","DOI":"10.4319\/lo.2013.58.6.1947"},{"key":"ref33","doi-asserted-by":"crossref","unstructured":"Klitgaard, A. B. and Tendal, O. S.: Distribution and species composition of\nmass occurrences of large-sized sponges in the northeast Atlantic, Prog.\nOceanogr., 61, 57\u201398, https:\/\/doi.org\/10.1016\/j.pocean.2004.06.002, 2004.","DOI":"10.1016\/j.pocean.2004.06.002"},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"Kutti, T., Bannister, R. J., and Fossa, J. H.: Community structure and\necological function of deep-water sponge grounds in the Traenadypet\nMPA-Northern Norwegian continental shelf, Cont. Shelf Res., 69, 21\u201330,\nhttps:\/\/doi.org\/10.1016\/j.csr.2013.09.011, 2013.","DOI":"10.1016\/j.csr.2013.09.011"},{"key":"ref35","doi-asserted-by":"crossref","unstructured":"Kutti, T., Bannister, R. J., Fossa, J. H., Krogness, C. M., Tjensvoll, I.,\nand Sovik, G.: Metabolic responses of the deep-water sponge Geodia barretti\nto suspended bottom sediment, simulated mine tailings and drill cuttings, J.\nExp. Mar. Biol. Ecol., 473, 64\u201372, https:\/\/doi.org\/10.1016\/j.jembe.2015.07.017, 2015.","DOI":"10.1016\/j.jembe.2015.07.017"},{"key":"ref36","doi-asserted-by":"crossref","unstructured":"Leys, S. P., Kahn, A. S., Fang, J. K. H., Kutti, T., and Bannister, R. J.:\nPhagocytosis of microbial symbionts balances the carbon and nitrogen budget\nfor the deep-water boreal sponge Geodia barretti, Limnol. Oceanogr., 63,\n187\u2013202, https:\/\/doi.org\/10.1002\/lno.10623, 2018.","DOI":"10.1002\/lno.10623"},{"key":"ref37","doi-asserted-by":"crossref","unstructured":"Li, Z. Y., Wang, Y. Z., He, L. M., and Zheng, H. J.: Metabolic profiles of\nprokaryotic and eukaryotic communities in deep-sea sponge Lamellomorpha sp\nindicated by metagenomics, Sci. Rep., 4, 1\u201311, https:\/\/doi.org\/10.1038\/srep03895, 2014.","DOI":"10.1038\/srep03895"},{"key":"ref38","doi-asserted-by":"crossref","unstructured":"Liu, F., Li, J. L., Feng, G. F., and Li, Z. Y.: New Genomic Insights into\n\u201cEntotheonella\u201d Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic\nAdaptation, Resilience, and Interaction, Front. Microbiol., 7, 1\u201311,\nhttps:\/\/doi.org\/10.3389\/fmicb.2016.01333, 2016.","DOI":"10.3389\/fmicb.2016.01333"},{"key":"ref39","doi-asserted-by":"crossref","unstructured":"Liu, M., Fan, L., Zhong, L., Kjelleberg, S., and Thomas, T.:\nMetaproteogenomic analysis of a community of sponge symbionts, Isme J.,\n6, 1515\u20131525, https:\/\/doi.org\/10.1038\/ismej.2012.1, 2012.","DOI":"10.1038\/ismej.2012.1"},{"key":"ref40","doi-asserted-by":"crossref","unstructured":"Maldonado, M., Ribes, M., and van Duyl, F. C.: Chapter three \u2013 Nutrient\nFluxes Through Sponges: Biology, Budgets, and Ecological Implications, in:\nAdvances in Marine Biology, edited by: Becerro, M. A., Uriz, M. J.,\nMaldonado, M., and Turon, X., Academic Press, 113\u2013182, 2012.","DOI":"10.1016\/B978-0-12-394283-8.00003-5"},{"key":"ref41","doi-asserted-by":"crossref","unstructured":"Marchant, H. K., Ahmerkamp, S., Lavik, G., Tegetmeyer, H. E., Graf, J.,\nKlatt, J. M., Holtappels, M., Walpersdorf, E., and Kuypers, M. M.:\nDenitrifying community in coastal sediments performs aerobic and anaerobic\nrespiration simultaneously, ISME J., 11, 1799\u20131812, 2017.","DOI":"10.1038\/ismej.2017.51"},{"key":"ref42","doi-asserted-by":"crossref","unstructured":"Mehta, M. P., Butterfield, D. A., and Baross, J. A.: Phylogenetic diversity\nof nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments\nof the Juan de Fuca ridge, Appl. Environ. Microbiol., 69, 960\u2013970,\nhttps:\/\/doi.org\/10.1128\/aem.69.2.960-970.2003, 2003.","DOI":"10.1128\/AEM.69.2.960-970.2003"},{"key":"ref43","doi-asserted-by":"crossref","unstructured":"Middelburg, J. J., Soetaert, K., Herman, P. M. J., and Heip, C. H. R.:\nDenitrification in marine sediments: A model study, Global Biogeochem.\nCy., 10, 661\u2013673, https:\/\/doi.org\/10.1029\/96GB02562, 1996.","DOI":"10.1029\/96GB02562"},{"key":"ref44","doi-asserted-by":"crossref","unstructured":"Mohamed, N., S Colman, A., Tal, Y., and Hill, R.: Diversity and expression\nof nitrogen fixation genes in bacterial symbionts of marine sponges,\nEnviron. Microbiol., 10, 2910\u20132921, https:\/\/doi.org\/10.1111\/j.1462-2920.2008.01704.x, 2008.","DOI":"10.1111\/j.1462-2920.2008.01704.x"},{"key":"ref45","doi-asserted-by":"crossref","unstructured":"Mohamed, N. M., Saito, K., Tal, Y., and Hill, R. T.: Diversity of aerobic\nand anaerobic ammonia-oxidizing bacteria in marine sponges, Isme J., 4,\n38\u201348, https:\/\/doi.org\/10.1038\/ismej.2009.84, 2010.","DOI":"10.1038\/ismej.2009.84"},{"key":"ref46","doi-asserted-by":"crossref","unstructured":"Murillo, F. J., Mu\u00f1oz, P. D., Cristobo, J., R\u00edos, P., Gonz\u00e1lez,\nC., Kenchington, E., and Serrano, A.: Deep-sea sponge grounds of the Flemish\nCap, Flemish Pass and the Grand Banks of Newfoundland (Northwest Atlantic\nOcean): Distribution and species composition, Mar. Biol. Res., 8, 842\u2013854, https:\/\/doi.org\/10.1080\/17451000.2012.682583, 2012.","DOI":"10.1080\/17451000.2012.682583"},{"key":"ref47","doi-asserted-by":"crossref","unstructured":"Nielsen, L. P.: Denitrification in sediment determined from nitrogen isotope\npairing, FEMS Microbiol. Ecol., 9, 357\u2013361, https:\/\/doi.org\/10.1111\/j.1574-6941.1992.tb01771.x, 1992.","DOI":"10.1111\/j.1574-6941.1992.tb01771.x"},{"key":"ref48","doi-asserted-by":"crossref","unstructured":"Osinga, R., Tramper, J., and Wijffels, R. H.: Cultivation of marine sponges,\nMar. Biotechnol., 1, 509\u2013532, https:\/\/doi.org\/10.1007\/Pl00011807, 1999.","DOI":"10.1007\/PL00011807"},{"key":"ref49","doi-asserted-by":"crossref","unstructured":"Osinga, R., Armstrong, E., Burgess, J. G., Hoffmann, F., Reitner, J., and\nSchumann-Kindel, G.: Sponge-microbe associations and their importance for\nsponge bioprocess engineering, Hydrobiologia, 461, 55\u201362, https:\/\/doi.org\/10.1023\/A:1012717200362, 2001.","DOI":"10.1023\/A:1012717200362"},{"key":"ref50","doi-asserted-by":"crossref","unstructured":"Painter, H.: A review of literature on inorganic nitrogen metabolism in\nmicroorganisms, Water Res., 4, 393\u2013450, https:\/\/doi.org\/10.1016\/0043-1354(70)90051-5, 1970.","DOI":"10.1016\/0043-1354(70)90051-5"},{"key":"ref51","doi-asserted-by":"crossref","unstructured":"Pawlik, J. R. and McMurray, S. E.: The Emerging Ecological and\nBiogeochemical Importance of Sponges on Coral Reefs, Ann. Rev. Mar.\nSci., 12, 315\u2013337, https:\/\/doi.org\/10.1146\/annurev-marine-010419-010807, 2019.","DOI":"10.1146\/annurev-marine-010419-010807"},{"key":"ref52","doi-asserted-by":"crossref","unstructured":"Pfannkuchen, M., Fritz, G. B., Schlesinger, S., Bayer, K., and Br\u00fcmmer,\nF.: In situ pumping activity of the sponge Aplysina aerophoba, Nardo 1886, J.\nExp. Mar. Biol. Ecol., 369, 65\u201371, https:\/\/doi.org\/10.1016\/j.jembe.2008.10.027, 2009.","DOI":"10.1016\/j.jembe.2008.10.027"},{"key":"ref53","doi-asserted-by":"crossref","unstructured":"Pita, L., Rix, L., Slaby, B. M., Franke, A., and Hentschel, U.: The sponge\nholobiont in a changing ocean: from microbes to ecosystems, Microbiome, 6,\n1\u201318, https:\/\/doi.org\/10.1186\/s40168-018-0428-1, 2018.","DOI":"10.1186\/s40168-018-0428-1"},{"key":"ref54","doi-asserted-by":"crossref","unstructured":"Radax, R., Hoffmann, F., Rapp, H. T., Leininger, S., and Schleper, C.:\nAmmonia-oxidizing archaea as main drivers of nitrification in cold-water\nsponges, Environ. Microbiol., 14, 909\u2013923, https:\/\/doi.org\/10.1111\/j.1462-2920.2011.02661.x, 2012.","DOI":"10.1111\/j.1462-2920.2011.02661.x"},{"key":"ref55","doi-asserted-by":"crossref","unstructured":"Reiswig, H. M.: Water transport, respiration and energetics of three\ntropical marine sponges, J. Exp. Mar. Biol. Ecol., 14, 231\u2013249, https:\/\/doi.org\/10.1016\/0022-0981(74)90005-7, 1974.","DOI":"10.1016\/0022-0981(74)90005-7"},{"key":"ref56","doi-asserted-by":"crossref","unstructured":"Ribes, M., Dziallas, C., Coma, R., and Riemann, L.: Microbial Diversity and\nPutative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean\nSponges, Appl. Environ. Microbiol., 81, 5683\u20135693, https:\/\/doi.org\/10.1128\/aem.01320-15, 2015.","DOI":"10.1128\/AEM.01320-15"},{"key":"ref57","doi-asserted-by":"crossref","unstructured":"Risgaard-Petersen, N., Nielsen, L. P., Rysgaard, S., Dalsgaard, T., and\nMeyer, R. L.: Application of the isotope pairing technique in sediments\nwhere anammox and denitrification coexist, Limnol. Oceanogr.-Method., 1, 63\u201373, https:\/\/doi.org\/10.4319\/lom.2003.1.63, 2003.","DOI":"10.4319\/lom.2003.1.63"},{"key":"ref58","doi-asserted-by":"crossref","unstructured":"Rix, L., de Goeij, J. M., Mueller, C. E., Struck, U., Middelburg, J. J., van\nDuyl, F. C., Al-Horani, F. A., Wild, C., Naumann, M. S., and van Oevelen,\nD.: Coral mucus fuels the sponge loop in warm- and cold-water coral reef\necosystems, Sci. Rep., 6, 18715, https:\/\/doi.org\/10.1038\/srep18715,\n2016.","DOI":"10.1038\/srep18715"},{"key":"ref59","doi-asserted-by":"crossref","unstructured":"Roberts, E. M., Mienis, F., Rapp, H. T., Hanz, U., Meyer, H. K., and Davies,\nA. J.: Oceanographic setting and short-timescale environmental variability\nat an Arctic seamount sponge ground, Deep-Sea Res. Pt. I, 138, 98\u2013113,\nhttps:\/\/doi.org\/10.1016\/j.dsr.2018.06.007, 2018.","DOI":"10.1016\/j.dsr.2018.06.007"},{"key":"ref60","doi-asserted-by":"crossref","unstructured":"Robertson, L. A., Dalsgaard, T., Revsbech, N. P., and Kuenen, J. G.:\nConfirmation of \u201caerobic denitrification\u201d in batch cultures, using\ngas-chromatography and 15 mass spectrometry, FEMS Microbiol. Ecol., 18,\n113\u2013119, https:\/\/doi.org\/10.1111\/j.1574-6941.1995.tb00168.x, 1995.","DOI":"10.1016\/0168-6496(95)00047-E"},{"key":"ref61","unstructured":"Rooks, C., Fang, J. K.-H., M\u00f8rkved, P. T., Zhao, R., Rapp, H. T., Xavier, J. R., and Hoffmann, F.: Denitrification rates in boreo-arctic sponges \u2013 data of sponge species from Korsfjord (Norway) and the Schulz Bank (Arctic Ocean), PANGAEA, https:\/\/doi.org\/10.1594\/PANGAEA.899821, 2019."},{"key":"ref62","doi-asserted-by":"crossref","unstructured":"Rysgaard, S., Christensen, P. B., and Nielsen, L. P.: Seasonal-Variation in\nNitrification and Denitrification in Estuarine Sediment Colonized by Benthic\nMicroalgae and Bioturbating Infauna, Mar. Ecol. Prog. Ser., 126, 111\u2013121, https:\/\/doi.org\/10.3354\/meps126111, 1995.","DOI":"10.3354\/meps126111"},{"key":"ref63","doi-asserted-by":"crossref","unstructured":"Schl\u00e4ppy, M.-L., Hoffmann, F., R\u00f8y, H., Wijffels, R. H., Mendola, D.,\nSidri, M., and de Beer, D.: Oxygen dynamics and flow patterns of Dysidea avara (Porifera: Demospongiae), J. Mar. Biol. Assoc. UK, 87, 1677\u20131682, https:\/\/doi.org\/10.1017\/S0025315407058146, 2007.","DOI":"10.1017\/S0025315407058146"},{"key":"ref64","doi-asserted-by":"crossref","unstructured":"Schl\u00e4ppy, M.-L., Sch\u00f6ttner, S. I., Lavik, G., Kuypers, M. M. M., de\nBeer, D., and Hoffmann, F.: Evidence of nitrification and denitrification in\nhigh and low microbial abundance sponges, Mar. Biol., 157, 593\u2013602, https:\/\/doi.org\/10.1007\/s00227-009-1344-5, 2010a.","DOI":"10.1007\/s00227-009-1344-5"},{"key":"ref65","doi-asserted-by":"crossref","unstructured":"Schl\u00e4ppy, M. L., Weber, M., Mendola, D., Hoffmann, F., and de Beer, D.:\nHeterogeneous oxygenation resulting from active and passive flow in two\nMediterranean sponges, Dysida avara and Chondrosia reniformis, Limnol.\nOceanogr., 55, 1289\u20131300, https:\/\/doi.org\/10.4319\/lo.2010.55.3.1289, 2010b.","DOI":"10.4319\/lo.2010.55.3.1289"},{"key":"ref66","doi-asserted-by":"crossref","unstructured":"Seitzinger, S. P.: Denitrification in freshwater and coastal marine\necosystems: Ecological and geochemical significance, Limnol. Oceanogr., 33,\n702\u2013724, https:\/\/doi.org\/10.4319\/lo.1988.33.4part2.0702, 1988.","DOI":"10.4319\/lo.1988.33.4part2.0702"},{"key":"ref67","doi-asserted-by":"crossref","unstructured":"Seitzinger, S. P. and Giblin, A. E.: Estimating denitrification in North\nAtlantic continental shelf sediments, Biogeochemistry, 35, 235\u2013260, https:\/\/doi.org\/10.1007\/Bf02179829, 1996.","DOI":"10.1007\/BF02179829"},{"key":"ref68","unstructured":"Shapleigh, J. P.: Denitrifying Prokaryotes, in: The Prokaryotes: Prokaryotic\nPhysiology and Biochemistry, edited by: Rosenberg, E., DeLong, E. F., Lory,\nS., Stackebrandt, E., and Thompson, F., Springer Berlin Heidelberg, Berlin,\nHeidelberg, 405\u2013425, 2013."},{"key":"ref69","doi-asserted-by":"crossref","unstructured":"Southwell, M. W., Popp, B. N., and Martens, C. S.: Nitrification controls on\nfluxes and isotopic composition of nitrate from Florida Keys sponges, Mar.\nChem., 108, 96\u2013108, https:\/\/doi.org\/10.1016\/j.marchem.2007.10.005, 2008.","DOI":"10.1016\/j.marchem.2007.10.005"},{"key":"ref70","doi-asserted-by":"crossref","unstructured":"Thamdrup, B. and Dalsgaard, T.: Production of N2 through anaerobic\nammonium oxidation coupled to nitrate reduction in marine sediments, Appl.\nEnviron. Microbiol., 68, 1312\u20131318, https:\/\/doi.org\/10.1128\/AEM.68.3.1312-1318.2002, 2002.","DOI":"10.1128\/AEM.68.3.1312-1318.2002"},{"key":"ref71","doi-asserted-by":"crossref","unstructured":"Throback, I. N., Enwall, K., Jarvis, A., and Hallin, S.: Reassessing PCR\nprimers targeting nirS, nirK and nosZ genes for community surveys of\ndenitrifying bacteria with DGGE, FEMS Microbiol. Ecol., 49, 401\u2013417,\nhttps:\/\/doi.org\/10.1016\/j.femsec.2004.04.011, 2004.","DOI":"10.1016\/j.femsec.2004.04.011"},{"key":"ref72","doi-asserted-by":"crossref","unstructured":"Tjensvoll, I., Kutti, T., Fossa, J. H., and Bannister, R. J.: Rapid\nrespiratory responses of the deep-water sponge Geodia barretti exposed to\nsuspended sediments, Aquat. Biol., 19, 65\u201373, https:\/\/doi.org\/10.3354\/ab00522, 2013.","DOI":"10.3354\/ab00522"},{"key":"ref73","doi-asserted-by":"crossref","unstructured":"Ward, B. B., Devol, A. H., Rich, J. J., Chang, B. X., Bulow, S. E., Naik,\nH., Pratihary, A., and Jayakumar, A.: Denitrification as the dominant\nnitrogen loss process in the Arabian Sea, Nature, 461, 78\u201381, https:\/\/doi.org\/10.1038\/nature08276, 2009.","DOI":"10.1038\/nature08276"},{"key":"ref74","doi-asserted-by":"crossref","unstructured":"Webster, N. S. and Taylor, M. W.: Marine sponges and their microbial\nsymbionts: love and other relationships, Environ. Microbiol., 14,\n335\u2013346, https:\/\/doi.org\/10.1111\/j.1462-2920.2011.02460.x, 2012.","DOI":"10.1111\/j.1462-2920.2011.02460.x"},{"key":"ref75","doi-asserted-by":"crossref","unstructured":"Weisz, J. B., Lindquist, N., and Martens, C. S.: Do associated microbial\nabundances impact marine demosponge pumping rates and tissue densities?,\nOecologia, 155, 367\u2013376, https:\/\/doi.org\/10.1007\/s00442-007-0910-0, 2008.","DOI":"10.1007\/s00442-007-0910-0"},{"key":"ref76","doi-asserted-by":"crossref","unstructured":"Wilkinson, C. R. and Fay, P.: Nitrogen fixation in coral reef sponges with\nsymbiotic cyanobacteria, Nature, 279, 527\u2013529, https:\/\/doi.org\/10.1038\/279527a0, 1979.","DOI":"10.1038\/279527a0"},{"key":"ref77","unstructured":"Wilkinson, C. R., Summons, R. E., and Evans, E.: Nitrogen fixation in\nsymbiotic marine sponges: Ecological significance and difficulties in\ndetection, 667\u2013673, 1999."},{"key":"ref78","doi-asserted-by":"crossref","unstructured":"Wilson, T. R. S.: Evidence for denitrification in aerobic pelagic sediments,\nNature, 274, 354\u2013356, https:\/\/doi.org\/10.1038\/274354a0, 1978.","DOI":"10.1038\/274354a0"},{"key":"ref79","doi-asserted-by":"crossref","unstructured":"Yahel, G., Sharp, J. H., Marie, D., H\u00e4se, C., and Genin, A.: In situ\nfeeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon, Limnol. Oceanogr., 48,\n141\u2013149, https:\/\/doi.org\/10.4319\/lo.2003.48.1.0141, 2003.","DOI":"10.4319\/lo.2003.48.1.0141"},{"key":"ref80","doi-asserted-by":"crossref","unstructured":"Zhang, F., Jonas, L., Lin, H., and Hill, R. T.: Microbially mediated\nnutrient cycles in marine sponges, FEMS Microbiol. Ecol., 95, 1\u201314,\nhttps:\/\/doi.org\/10.1093\/femsec\/fiz155, 2019.","DOI":"10.1093\/femsec\/fiz155"},{"key":"ref81","doi-asserted-by":"crossref","unstructured":"Zhang, X., He, L. M., Zhang, F. L., Sun, W., and Li, Z. Y.: The Different\nPotential of Sponge Bacterial Symbionts in N2 Release Indicated by the\nPhylogenetic Diversity and Abundance Analyses of Denitrification Genes, nirK\nand nosZ, Plos One, 8, e65142, https:\/\/doi.org\/10.1371\/journal.pone.0065142, 2013.","DOI":"10.1371\/journal.pone.0065142"},{"key":"ref82","doi-asserted-by":"crossref","unstructured":"Zhuang, L. P., Lin, B. B., Qin, F., and Luo, L. Z.: Zhouia spongiae sp nov.,\nisolated from a marine sponge, Int. J. System.\nEvolut. Microbiol., 68, 2194\u20132198, https:\/\/doi.org\/10.1099\/ijsem.0.002808, 2018.","DOI":"10.1099\/ijsem.0.002808"}],"container-title":["Biogeosciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/bg.copernicus.org\/articles\/17\/1231\/2020\/bg-17-1231-2020.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,31]],"date-time":"2025-01-31T21:29:02Z","timestamp":1738358942000},"score":1,"resource":{"primary":{"URL":"https:\/\/bg.copernicus.org\/articles\/17\/1231\/2020\/"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,6]]},"references-count":82,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020]]}},"URL":"https:\/\/doi.org\/10.5194\/bg-17-1231-2020","relation":{"has-preprint":[{"id-type":"doi","id":"10.5194\/bg-2019-135","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135","asserted-by":"object"}],"has-review":[{"id-type":"doi","id":"10.5194\/bg-2019-135-RC1","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC2","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-RC2","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC3","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-RC3","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC4","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC1","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC5","asserted-by":"subject"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC4","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC5","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-RC1","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-RC2","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-RC3","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC1","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC2","asserted-by":"object"},{"id-type":"doi","id":"10.5194\/bg-2019-135-AC3","asserted-by":"object"}],"is-part-of":[{"id-type":"doi","id":"10.1594\/PANGAEA.899821","asserted-by":"subject"}]},"ISSN":["1726-4189"],"issn-type":[{"value":"1726-4189","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,6]]}}}